192
Views
16
CrossRef citations to date
0
Altmetric
Review

Group B coxsackieviruses and autoimmunity: focus on Type 1 diabetes

, &
Pages 357-366 | Published online: 10 Jan 2014

References

  • Selmi C. Autoimmunity in 2009. Autoimmun. Rev.9(12), 795–800 (2010).
  • Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med.347(12), 911–920 (2002).
  • Goldberg E, Krause I. Infection and Type 1 diabetes mellitus – a two edged sword? Autoimmun. Rev.8(8), 682–686 (2009).
  • Hober D, Sane F. Enteroviral pathogenesis of Type 1 diabetes. Discov. Med.10(51), 151–160 (2010).
  • Pallansch MA, Roos RP, Knipe DM. Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses. In: Fields Virology 2007 (5th Ed.). Lippincott Williams & Wilkins, PA, USA, 839–894 (2006).
  • Oberste MS. Comparative genomics of the coxsackie B viruses and related enteroviruses. Curr. Top. Microbiol. Immunol.323, 33–47 (2008).
  • Kallewaard NL, Zhang L, Chen JW, Guttenberg M, Sanchez MD, Bergelson JM. Tissue-specific deletion of the coxsackievirus and adenovirus receptor protects mice from virus-induced pancreatitis and myocarditis. Cell Host Microbe.6(1), 91–98 (2009).
  • Tracy S, Oberste MS, Drescher KM. Group B coxsackieviruses. In: Current Topics in Microbiology and Immunology (Volume 323). Springer, Berlin, Germany 293–309 (2008).
  • Jaïdane H, Hober D. Role of coxsackievirus B4 in the pathogenesis of Type 1 diabetes. Diabetes Metab.34(6 Pt 1), 537–548 (2008).
  • Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human Type 1 diabetes. Diabetologia52(6), 1143–1151 (2009).
  • Knowlton KU. CVB infection and mechanisms of viral cardiomyopathy. Curr. Top. Micobiol. Immunol.323, 315–335 (2008).
  • Ylipaasto P, Klingel K, Lindberg AM et al. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet β cells. Diabetologia47(2), 225–39 (2004).
  • Chehadeh W, Kerr-Conte J, Pattou F et al. Persistent infection of human pancreatic islets by coxsackievirus B is associated with α interferon synthesis in β cells. J. Virol.74(21), 10153–10164 (2000).
  • Feuer R, Mena I, Pagarigan R, Slifka MK, Whitton JL. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J. Virol.76(9), 4430–4440 (2002).
  • Chaplin DD. Overview of the immune response. J. Allergy Clin. Immunol.125(2 Suppl. 2), S3–S23 (2010).
  • Ylipaasto P, Kutlu B, Rasilainen S et al. Global profiling of coxsackievirus- and cytokine-induced gene expression in human pancreatic islets. Diabetologia48(8), 1510–1522 (2005).
  • Rasschaert J, Ladrière L, Urbain M et al. Toll-like receptor 3 and STAT-1 contribute to double-stranded RNA+ interferon-γ-induced apoptosis in primary pancreatic β-cells. J. Biol. Chem.280(40), 33984–33991 (2005).
  • Dogusan Z, García M, Flamez D et al. Double-stranded RNA induces pancreatic β-cell apoptosis by activation of the Toll-like receptor 3 and interferon regulatory factor 3 pathways. Diabetes57(5), 1236–1245 (2008).
  • Haller O, Kochs G, Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology344(1), 119–130 (2006).
  • Hühn MH, McCartney SA, Lind K, Svedin E, Colonna M, Flodström-Tullberg M. Melanoma differentiation-associated protein-5 (MDA-5) limits early viral replication but is not essential for the induction of type 1 interferons after coxsackievirus infection. Virology401(1), 42–48 (2010).
  • Nejentsev S, Walker N, Riches D, Egholm M, Todd JA. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against Type 1 diabetes. Science324(5925), 387–389 (2009).
  • Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and β-cell loss in Type 1 diabetes. Nat. Rev. Endocrinol.5(4), 219–226 (2009).
  • Triantafilou K, Orthopoulos G, Vakakis E et al. Human cardiac inflammatory responses triggered by coxsackie B viruses are mainly Toll-like receptor (TLR) 8-dependent. Cell Microbiol.7(8), 1117–1126 (2005).
  • Wang JP, Asher DR, Chan M, Kurt-Jones EA, Finberg RW. Cutting edge: antibody-mediated TLR7-dependent recognition of viral RNA. J. Immunol.178(6), 3363–3367 (2007).
  • Richer MJ, Lavallée DJ, Shanina I, Horwitz MS. Toll-like receptor 3 signaling on macrophages is required for survival following coxsackievirus B4 infection. PLoS ONE4(1), e4127 (2009).
  • Hultcrantz M, Hühn MH, Wolf M et al. Interferons induce an antiviral state in human pancreatic islet cells. Virology367(1), 92–101 (2007).
  • Hühn MH, Hultcrantz M, Lind K, Ljunggren HG, Malmberg KJ, Flodström-Tullberg M. IFN-γ production dominates the early human natural killer cell response to coxsackievirus infection. Cell Microbiol.10(2), 426–436 (2008).
  • von Herrath M. Diabetes: a virus-gene collaboration. Nature459(7246), 518–519 (2009).
  • Hühn MH, McCartney SA, Lind K, Svedin E, Colonna M, Flodström-Tullberg M. Melanoma differentiation-associated protein-5 (MDA-5) limits early viral replication but is not essential for the induction of type 1 interferons after coxsackievirus infection. Virology401(1), 42–48 (2010).
  • Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J, Whitton JL. The role of B lymphocytes in coxsackievirus B3 infection. Am. J. Pathol.155(4), 1205–1215 (1999).
  • Misbah SA, Spickett GP, Ryba PC, Hockaday JM, Kroll JS, Sherwood C. Chronic enteroviral meningoencephalitis in agammaglobulinemia: case report and literature review. J. Clin. Immunol.12(4), 266–270 (1992).
  • Schmugge M, Lauener R, Bossart W, Seger RA, Güngör T. Chronic enteroviral meningo-encephalitis in X-linked agammaglobulinaemia: favourable response to anti-enteroviral treatment. Eur. J. Pediatr.158(12), 1010–1011 (1999).
  • Henke A, Huber S, Stelzner A, Whitton JL. The role of CD8+ T lymphocytes in coxsackievirus B3-induced myocarditis. J. Virol.69(11), 6720–6728 (1995).
  • Skarsvik S, Puranen J, Honkanen J et al. Decreased in vitro type 1 immune response against coxsackie virus B4 in children with Type 1 diabetes. Diabetes55(4), 996–1003 (2006).
  • Hober D, Sauter P. Pathogenesis of Type 1 diabetes mellitus: interplay between enterovirus and host. Nat. Rev. Endocrinol.6(5), 279–289 (2010).
  • Tauriainen S, Oikarinen S, Oikarinen M, Hyöty H. Enteroviruses in the pathogenesis of Type 1 diabetes. Semin. Immunopathol.33(1), 45–55 (2010).
  • Hober D, Sane F. Enteroviruses and Type 1 diabetes. Br. Med. J.3, 342 (2011).
  • Yeung WC, Rawlinson WD, Craig ME. Enterovirus infection and Type 1 diabetes mellitus: systematic review and meta-analysis of observational molecular studies. Br. Med. J.3, 342 (2011).
  • Jaïdane H, Sauter P, Sane F, Goffard A, Gharbi J, Hober D. Enteroviruses and Type 1 diabetes: towards a better understanding of the relationship. Rev. Med. Virol.20(5), 265–280 (2010).
  • Di Lorenzo TP, Peakman M, Roep BO. Translational mini-review series on Type 1 diabetes: systematic analysis of T cell epitopes in autoimmune diabetes. Clin. Exp. Immunol.148(1), 1–16 (2007).
  • Mariño E, Batten M, Groom J et al. Marginal-zone B-cells of nonobese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes57(2), 395–404 (2008).
  • Haverkos HW, Battula N, Drotman DP, Rennert OM. Enteroviruses and Type 1 diabetes mellitus. Biomed. Pharmacother.57(9), 379–385 (2003).
  • Green J, Casabonne D, Newton R. Coxsackie B virus serology and Type 1 diabetes mellitus: a systematic review of published case–control studies. Diabet. Med.21, 507–514 (2004).
  • Gamble DR, Kinsley MJ, Fitzgerald MG et al. Viral antibodies in diabetes mellitus. Br. Med. J.3, 627–630 (1969).
  • Yoon JW, Austin M, Onodera T et al. Isolation of a virus from the pancreas of a child with diabetic ketoacidosis (virus-induced diabetes mellitus). N. Engl. J. Med.300, 1173–1179 (1979).
  • Andréoletti L, Hober D, Hober-Vandenberghe C et al. Detection of coxsackie B virus RNA sequences in whole blood samples from adult patients at the onset of Type I diabetes mellitus. J. Med. Virol.52(2), 121–127 (1997).
  • Schulte BM, Bakkers J, Lanke KH et al. Detection of enterovirus RNA in peripheral blood mononuclear cells of Type 1 diabetic patients beyond the stage of acute infection. Viral Immunol.23(1), 99–104 (2010).
  • Toniolo A, Maccari G, Federico G, Salvatoni A, Bianchi G, Baj A. Are enterovirus infections linked to the early stages of Type 1 diabetes? Presented at: American Society for Microbiology Meeting. San Diego, CA, USA, 23–27 May 2010 (Abstract).
  • Yin H, Berg AK, Tuvemo T, Frisk G. Enterovirus RNA is found in peripheral blood mononuclear cells in a majority of Type 1 diabetic children at onset. Diabetes51(6), 1964–1971 (2002).
  • Moya-Suri V, Schlosser M, Zimmermann K, Rjasanowski I, Gürtler L, Mentel R. Enterovirus RNA sequences in sera of schoolchildren in the general population and their association with Type 1-diabetes-associated autoantibodies. J. Med. Microbiol.54(Pt 9), 879–883 (2005).
  • Kawashima H, Ihara T, Ioi H et al. Enterovirus-related Type 1 diabetes mellitus and antibodies to glutamic acid decarboxylase in Japan. J. Infect.49(2), 147–151 (2004).
  • Salminen KK, Vuorinen T, Oikarinen S et al. Isolation of enterovirus strains from children with preclinical Type 1 diabetes. Diabet. Med.21(2), 156–164 (2004).
  • Dotta F, Censini S, van Halteren AG et al. Coxsackie B4 virus infection of β cells and natural killer cell insulitis in recent-onset Type 1 diabetic patients. Proc. Natl Acad. Sci. USA104(12), 5115–5120 (2007).
  • Sadeharju K, Hämäläinen AM, Knip M et al. Enterovirus infections as a risk factor for Type I diabetes: virus analyses in a dietary intervention trial. Clin. Exp. Immunol.132(2), 271–277 (2003).
  • Sarmiento L, Cabrera-Rode E, Lekuleni L et al. Occurrence of enterovirus RNA in serum of children with newly diagnosed Type 1 diabetes and islet cell autoantibody-positive subjects in a population with a low incidence of Type 1 diabetes. Autoimmunity40(7), 540–545 (2007).
  • Oikarinen M, Tauriainen S, Honkanen T et al. Detection of enteroviruses in the intestine of Type 1 diabetic patients. Clin. Exp. Immunol.151(1), 71–75 (2007).
  • Roivainen M, Klingel K. Role of enteroviruses in the pathogenesis of Type 1 diabetes. Diabetologia52(6), 995–996 (2009).
  • Tracy S, Drescher KM. Coxsackievirus infections and NOD mice: relevant models of protection from, and induction of, Type 1 diabetes. Ann. NY Acad. Sci.1103, 143–151 (2007).
  • Elfving M, Svensson J, Oikarinen S et al. Maternal enterovirus infection during pregnancy as a risk factor in offspring diagnosed with Type 1 diabetes between 15 and 30 years of age. Exp. Diabetes Res.2008, 271958 (2008).
  • Lönnrot M, Salminen K, Knip M et al. Enterovirus RNA in serum is a risk factor for β-cell autoimmunity and clinical Type 1 diabetes: a prospective study. Childhood Diabetes in Finland (DiMe) Study Group. J. Med. Virol.61(2), 214–220 (2000).
  • Lönnrot M, Korpela K, Knip M et al. Enterovirus infection as a risk factor for β-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study. Diabetes49(8), 1314–1318 (2000).
  • Oikarinen S, Martiskainen M, Tauriainen S et al. Enterovirus RNA in blood is linked to the development of Type 1 diabetes. Diabetes60(1), 276–279 (2011).
  • Jaidane H, Sané F, Gharbi J, Aouni M, Romond MB, Hober D. Coxsackievirus B4 and Type 1 diabetes pathogenesis: contribution of animal models. Diabetes Metab. Res. Rev.25, 591–603 (2009).
  • Foulis AK, Farquharson MA, Meager A. Immunoreactive α-interferon in insulin-secreting β cells in Type 1 diabetes mellitus. Lancet2(8573), 1423–1427 (1987).
  • Huang X, Yuang J, Goddard A et al. Interferon expression in the pancreases of patients with Type I diabetes. Diabetes44(6), 658–664 (1995).
  • See DM, Tilles JG. Pathogenesis of virus-induced diabetes in mice. J. Infect. Dis.171(5), 1131–1138 (1995).
  • Hyöty H. Enterovirus infections and Type 1 diabetes. Ann. Med.34(3), 138–147 (2002).
  • Yin H, Berg AK, Westman J, Hellerström C, Frisk G. Complete nucleotide sequence of a coxsackievirus B-4 strain capable of establishing persistent infection in human pancreatic islet cells: effects on insulin release, proinsulin synthesis, and cell morphology. J. Med. Virol.68(4), 544–557 (2002).
  • Roivainen M, Ylipaasto P, Savolainen C, Galama J, Hovi T, Otonkoski T. Functional impairment and killing of human β cells by enteroviruses: the capacity is shared by a wide range of serotypes, but the extent is a characteristic of individual virus strains. Diabetologia45(5), 693–702 (2002).
  • Stewart TA, Hultgren B, Huang X, Pitts-Meek S, Hully J, MacLachlan NJ. Induction of Type I diabetes by interferon-α in transgenic mice. Science260(5116), 1942–1946 (1993).
  • Tam PE, Messner RP. Molecular mechanisms of coxsackievirus persistence in chronic inflammatory myopathy: viral RNA persists through formation of a double-stranded complex without associated genomic mutations or evolution. J. Virol.73(12), 10113–10121 (1999).
  • Duncan G, Pelletier I, Colbère-Garapin F. Two amino acid substitutions in the type 3 poliovirus capsid contribute to the establishment of persistent infection in HEp-2c cells by modifying virus–receptor interactions. Virology241(1), 14–29 (1998).
  • Horwitz MS, Bradley LM, Harbertson J, Krahl T, Lee J, Sarvetnick N. Diabetes induced by coxsackie virus: initiation by bystander damage and not molecular mimicry. Nat. Med.4(7), 781–785 (1998).
  • Serreze DV, Ottendorfer EW, Ellis TM, Gauntt CJ, Atkinson MA. Acceleration of Type 1 diabetes by a coxsackievirus infection requires a preexisting critical mass of autoreactive T-cells in pancreatic islets. Diabetes49(5), 708–711 (2000).
  • Horwitz MS, Fine C, Ilic A, Sarvetnick N. Requirements for viral-mediated autoimmune diabetes: β-cell damage and immune infiltration. J. Autoimmun.16(3), 211–217 (2001).
  • Horwitz MS, Ilic A, Fine C, Rodriguez E, Sarvetnick N. Presented antigen from damaged pancreatic β cells activates autoreactive T cells in virus-mediated autoimmune diabetes. J. Clin. Invest.109(1), 79–87 (2002).
  • Rasche S, Busick RY, Quinn A. GAD65-specific cytotoxic T lymphocytes mediate β-cell death and loss of function. Rev. Diabet. Stud.6(1), 43–53 (2009).
  • Kaufman DL, Clare-Salzler M, Tian J et al. Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes. Nature366(6450), 69–72 (1993).
  • Tisch R, Yang XD, Singer SM, Liblau RS, Fugger L, McDevitt HO. Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice. Nature366(6450), 72–75 (1993).
  • Horwitz MS, Sarvetnick N. Viruses, host responses, and autoimmunity. Immunol. Rev.169, 241–253 (1999).
  • Filippi CM, von Herrath MG. Viral trigger for Type 1 diabetes: pros and cons. Diabetes57(11), 2863–2871 (2008).
  • Payton MA, Hawkes CJ, Christie MR. Relationship of the 37,000- and 40,000-M(r) tryptic fragments of islet antigens in insulin-dependent diabetes to the protein tyrosine phosphatase-like molecule IA-2 (ICA512). J. Clin. Invest.96(3), 1506–1511 (1995).
  • Elias D, Markovits D, Reshef T, van der Zee R, Cohen IR. Induction and therapy of autoimmune diabetes in the non-obese diabetic (NOD/Lt) mouse by a 65-kDa heat shock protein. Proc. Natl Acad. Sci. USA87(4), 1576–1580 (1990).
  • Härkönen T, Lankinen H, Davydova B, Hovi T, Roivainen M. Enterovirus infection can induce immune responses that cross-react with β-cell autoantigen tyrosine phosphatase IA-2/IAR. J. Med. Virol.66, 340–350 (2002).
  • Christen U, Edelmann KH, McGavern DB, Wolfe T, Coon B, Teague MK. A viral epitope that mimics a self antigen can accelerate but not initiate autoimmune diabetes. J. Clin. Invest.114(9), 1290–1298 (2004).
  • Geenen V, Mottet M, Dardenne O et al. Thymic self-antigens for the design of a negative/tolerogenic self-vaccination against Type 1 diabetes. Curr. Opin. Pharmacol.10(4), 461–472 (2010).
  • Kecha-Kamoun O, Achour I, Martens H et al. Thymic expression of insulin-related genes in an animal model of autoimmune Type 1 diabetes. Diabetes Metab. Res. Rev.17(2), 146–152 (2001).
  • Geenen V, Kroemer G. Multiple ways to cellular immune tolerance. Immunol. Today14(12), 573–575 (1993).
  • Chatterjee NK, Hou J, Dockstader P, Charbonneau T. Coxsackievirus B4 infection alters thymic, splenic, and peripheral lymphocyte repertoire preceding onset of hyperglycemia in mice. J. Med. Virol.38(2), 124–131 (1993).
  • Brilot F, Chehadeh W, Charlet-Renard C, Martens H, Geenen V, Hober D. Persistent infection of human thymic epithelial cells by coxsackievirus B4. J. Virol.76(10), 5260–5265 (2002).
  • Jaïdane H, Gharbi J, Lobert PE et al. Prolonged viral RNA detection in blood and lymphoid tissues from coxsackievirus B4 E2 orally-inoculated Swiss mice. Microbiol. Immunol.50(12), 971–974 (2006).
  • Brilot F, Geenen V, Hober D, Stoddart CA. Coxsackievirus B4 infection of human fetal thymus cells. J. Virol.78(18), 9854–9861 (2004).
  • Brilot F, Jaïdane H, Geenen V, Hober D. Coxsackievirus B4 infection of murine foetal thymus organ cultures. J. Med. Virol.80(4), 659–66 (2008).
  • Takada A, Kawaoka Y. Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications. Rev. Med. Virol.13(6), 387–398 (2003).
  • Hober D, Chehadeh W, Bouzidi A, Wattré P. Antibody-dependent enhancement of coxsackievirus B4 infectivity of human peripheral blood mononuclear cells results in increased interferon-α synthesis. J. Infect. Dis.184(9), 1098–1108 (2001).
  • Chehadeh W, Bouzidi A, Alm G, Wattré P, Hober D. Human antibodies isolated from plasma by affinity chromatography increase the coxsackievirus B4-induced synthesis of interferon-α by human peripheral blood mononuclear cells in vitro. J. Gen. Virol.82(Pt 8), 1899–1907 (2001).
  • Sauter P, Lobert PE, Lucas B et al. Role of the capsid protein VP4 in the plasma-dependent enhancement of the coxsackievirus B4E2-infection of human peripheral blood cells. Virus Res.125(2), 183–190 (2007).
  • Hober D, Chehadeh W, Weill J et al. Circulating and cell-bound antibodies increase coxsackievirus B4-induced production of IFN-α by peripheral blood mononuclear cells from patients with Type 1 diabetes. J. Gen. Virol.83(Pt 9), 2169–2176 (2002).
  • Chehadeh W, Lobert PE, Sauter P et al. Viral protein VP4 is a target of human antibodies enhancing coxsackievirus B4- and B3-induced synthesis of α interferon. J. Virol.79(22), 13882–13891 (2005).
  • Sauter P, Chehadeh W, Lobert PE et al. A part of the VP4 capsid protein exhibited by coxsackievirus B4 E2 is the target of antibodies contained in plasma from patients with Type 1 diabetes. J. Med. Virol.80(5), 866–878 (2008).
  • Kishimoto C, Kurokawa M, Ochiai H. Antibody-mediated immune enhancement in coxsackievirus B3 myocarditis. J. Mol. Cell. Cardiol.34(9), 1227–1238 (2002).
  • Girn J, Kavoosi M, Chantler J. Enhancement of coxsackievirus B3 infection by antibody to a different coxsackievirus strain. J. Gen. Virol.83(Pt 2), 351–358 (2002).
  • Sauter P, Hober D. Mechanisms and results of the antibody-dependent enhancement of viral infections and role in the pathogenesis of coxsackievirus B-induced diseases. Microbes Infect.11(4), 443–445 (2009). Erratum in: Microbes Infect.11(14–15), 1219 (2009).
  • Tracy S, Drescher KM, Chapman NM et al. Toward testing the hypothesis that group B coxsackieviruses (CVB) trigger insulin-dependent diabetes: inoculating nonobese diabetic mice with CVB markedly lowers diabetes incidence. J. Virol.76(23), 12097–12111 (2002).
  • Filippi CM, Estes EA, Oldham JE, von Herrath MG. Immunoregulatory mechanisms triggered by viral infections protect from Type 1 diabetes in mice. J. Clin. Invest.119(6), 1515–1523 (2009).
  • Tracy S, Höfling K, Pirruccello S, Lane PH, Reyna SM, Gauntt CJ. Group B coxsackievirus myocarditis and pancreatitis: connection between viral virulence phenotypes in mice. J. Med. Virol.62(1), 70–81 (2000).
  • Drescher KM, Kono K, Bopegamage S, Carson SD, Tracy S. Coxsackievirus B3 infection and Type 1 diabetes development in NOD mice: insulitis determines susceptibility of pancreatic islets to virus infection. Virology329(2), 381–394 (2004).
  • Bach JF. Infections and autoimmune diseases. J. Autoimmun.25(Suppl.), 74–80 (2005).
  • Tracy S, Drescher KM, Jackson JD, Kim K, Kono K. Enteroviruses, Type 1 diabetes and hygiene: a complex relationship. Rev. Med. Virol.20(2), 106–116 (2010).
  • TEDDY Study Group. The Environmental Determinents of Diabetes in the Young (TEDDY) study: study design. Pediatr. Diabetes8, 286–298 (2007).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.